Orbitofrontal cortex governs working memory for temporal order

abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory, which may contribute to confabulation in individuals with OFC damage. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage may relate to impaired temporal-order understanding.

authors:

• Elizabeth L Johnson

• William K Chang

• Callum D Dewar

• Donna Sorensen

• Jack J Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G Larsson

• Jugoslav Ivanovic

• Torstein R Meling

• Donatella Scabini

• Robert T Knight

Date: 2022

DOI: https:// doi.org/10.1016/j.cub.2022.03.074.

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Orbitofrontal cortex governs working memory for temporal order

Abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory1, which may contribute to confabulation in individuals with OFC damage2. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage2 may relate to impaired temporal-order understanding.

Authors:

• Elizabeth L. Johnson

• William K. Chang

• Callum D. Dewar

• Donna Sorensen

• Jack J. Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G. Larsson

• Jugoslav Ivanovic

• Torstein R. Meling

• Donatella Scabini

• Robert T. Knight

Date: 2022

DOI: https://doi.org/10.1016/j.cub.2022.03.074

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Integrated analysis of anatomical and electrophysiological human intracranial data

ABSTRACT

Human intracranial electroencephalography (iEEG) recordings provide data with much greater spatiotemporal precision than is possible from data obtained using scalp EEG, magnetoencephalography (MEG), or functional MRI. Until recently, the fusion of anatomical data (MRI and computed tomography (CT) images) with electrophysiological data and their subsequent analysis have required the use of technologically and conceptually challenging combinations of software. Here, we describe a comprehensive protocol that enables complex raw human iEEG data to be converted into more readily comprehensible illustrative representations. The protocol uses an open-source toolbox for electrophysiological data analysis (FieldTrip). This allows iEEG researchers to build on a continuously growing body of scriptable and reproducible analysis methods that, over the past decade, have been developed and used by a large research community. In this protocol, we describe how to analyze complex iEEG datasets by providing an intuitive and rapid approach that can handle both neuroanatomical information and large electrophysiological datasets. We provide a worked example using an example dataset. We also explain how to automate the protocol and adjust the settings to enable analysis of iEEG datasets with other characteristics. The protocol can be implemented by a graduate student or postdoctoral fellow with minimal MATLAB experience and takes approximately an hour to execute, excluding the automated cortical surface extraction.

AUTHORS

• Arjen Stolk

• Sandon Griffin

• Roemer van der Meij

• Callum Dewar

• Ignacio Saez

• Jack J. Lin

• Giovanni Piantoni

• Jan-Mathijs Schoffelen

• Robert T. Knight 

• Robert Oostenveld 

Date: 2018

DOI: 10.1038/s41596-018-0009-6

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Bidirectional frontoparietal oscillatory systems support working memory

ABSTRACT

The ability to represent and select information in working memory provides the neurobiological infrastructure for human cognition. For 80 years, dominant views of working memory have focused on the key role of prefrontal cortex (PFC). However, more recent work has implicated posterior cortical regions, suggesting that PFC engagement during working memory is dependent on the degree of executive demand. We provide evidence from neurological patients with discrete PFC damage that challenges the dominant models attributing working memory to PFC-dependent systems. We show that neural oscillations, which provide a mechanism for PFC to communicate with posterior cortical regions, independently subserve communications both to and from PFC—uncovering parallel oscillatory mechanisms for working memory. Fourteen PFC patients and 20 healthy, age-matched controls performed a working memory task where they encoded, maintained, and actively processed information about pairs of common shapes. In controls, the electroencephalogram (EEG) exhibited oscillatory activity in the low-theta range over PFC and directional connectivity from PFC to parieto-occipital regions commensurate with executive processing demands. Concurrent alpha-beta oscillations were observed over parieto-occipital regions, with directional connectivity from parieto-occipital regions to PFC, regardless of processing demands. Accuracy, PFC low-theta activity, and PFC / parieto-occipital connectivity were attenuated in patients, revealing a PFC-independent, alpha-beta system. The PFC patients still demonstrated task proficiency, which indicates that the posterior alpha-beta system provides sufficient resources for working memory. Taken together, our findings reveal neurologically dissociable PFC and parieto-occipital systems and suggest that parallel, bidirectional oscillatory systems form the basis of working memory.

AUTHORS

• Elizabeth L. Johnson

• Callum Dewar

• Anne-Kristin Solbakk

• Tor Endestad

• Torstein Meling

• Robert T. Knight

Date: 2017

DOI: 10.1016/j.cub.2017.05.046

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Effects of prefrontal cortex damage on emotion understanding: EEG and behavioural evidence

ABSTRACT

Humans are highly social beings that interact with each other on a daily basis. In these complex interactions, we get along by being able to identify others’ actions and infer their intentions, thoughts and feelings. One of the major theories accounting for this critical ability assumes that the understanding of social signals is based on a primordial tendency to simulate observed actions by activating a mirror neuron system. If mirror neuron regions are important for action and emotion recognition, damage to regions in this network should lead to deficits in these domains. In the current behavioural and EEG study, we focused on the lateral prefrontal cortex including dorsal and ventral prefrontal cortex and utilized a series of task paradigms, each measuring a different aspect of recognizing others’ actions or emotions from body cues. We examined 17 patients with lesions including (n = 8) or not including (n = 9) the inferior frontal gyrus, a core mirror neuron system region, and compared their performance to matched healthy control subjects (n = 18), in behavioural tasks and in an EEG observation—execution task measuring mu suppression. Our results provide support for the role of the lateral prefrontal cortex in understanding others’ emotions, by showing that even unilateral lesions result in deficits in both accuracy and reaction time in tasks involving the recognition of others’ emotions. In tasks involving the recognition of actions, patients showed a general increase in reaction time, but not a reduction in accuracy. Deficits in emotion recognition can be seen by either direct damage to the inferior frontal gyrus, or via damage to dorsal lateral prefrontal cortex regions, resulting in deteriorated performance and less EEG mu suppression over sensorimotor cortex.

AUTHORS

• Anat Perry

• Samantha N. Saunders

• Jennifer Stiso

• Callum Dewar

• James Lubell

• Torstein Meling

• Anne-Kristin Solbakk

• Tor Endestad

• Robert T. Knight

Date: 2017

DOI: 10.1093/brain/awx031

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Direct brain recordings reveal hippocampal rhythm underpinnings of language processing

ABSTRACT

Language is classically thought to be supported by perisylvian cortical regions. Here we provide intracranial evidence linking the hippocampal complex to linguistic processing. We used direct recordings from the hippocampal structures to investigate whether theta oscillations, pivotal in memory function, track the amount of contextual linguistic information provided in sentences. Twelve participants heard sentences that were either constrained (“She locked the door with the”) or unconstrained (“She walked in here with the”) before presentation of the final word (“key”), shown as a picture that participants had to name. Hippocampal theta power increased for constrained relative to unconstrained contexts during sentence processing, preceding picture presentation. Our study implicates hippocampal theta oscillations in a language task using natural language associations that do not require memorization. These findings reveal that the hippocampal complex contributes to language in an active fashion, relating incoming words to stored semantic knowledge, a necessary process in the generation of sentence meaning.

AUTHORS

• Vitoria Piai

• Kristopher L. Anderson

• Jack J. Lin

• Callum Dewar

• Josef Parvizi

• Nina F. Dronkers

• Robert T. Knight

Date: 2016

DOI: www.pnas.org/cgi/doi/10.1073/pnas.1603312113

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The role of the orbitofrontal cortex in regulation of interpersonal space: evidence from frontal lesion and frontotemporal dementia patients

ABSTRACT

Interpersonal distance is central to communication and complex social behaviors but the neural correlates of interpersonal distance preferences are not defined. Previous studies suggest that damage to the orbitofrontal cortex (OFC) is associated with impaired interpersonal behavior. To examine whether the OFC is critical for maintaining appropriate interpersonal distance, we tested two groups of patients with OFC damage: Patients with OFC lesions and patients with behavioral variant frontotemporal dementia. These two groups were compared to healthy controls and to patients with lesions restricted to the dorsolateral prefrontal cortex. Only patients with OFC damage showed abnormal interpersonal distance preferences, which were significantly different from both controls and patients with dorsolateral prefrontal damage. The comfortable distances these patients chose with strangers were significantly closer than the other groups and resembled distances normally used with close others. These results shed light on the role of the OFC in regulating social behavior and may serve as a simple diagnostic tool for dementia or lesion patients.

AUTHORS

• Anat Perry

• Sandy J. Lwi

• Alice Verstaen

• Callum Dewar

• Robert W. Levenson

• Robert T. Knight

Date: 2016

DOI: 10.1093/scan/nsw109

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Hierarchy of prediction errors for auditory events in human temporal and frontal cortex

ABSTRACT

Predictive coding theories posit that neural networks learn statistical regularities in the environment for comparison with actual outcomes, signaling a prediction error (PE) when sensory deviation occurs. PE studies in audition have capitalized on low-frequency event-related potentials (LF-ERPs), such as the mismatch negativity. However, local cortical activity is well-indexed by higher-frequency bands [high-γ band (Hγ): 80–150 Hz]. We compared patterns of human Hγ and LF-ERPs in deviance detection using electrocorticographic recordings from subdural electrodes over frontal and temporal cortices. Patients listened to trains of task-irrelevant tones in two conditions differing in the predictability of a deviation from repetitive background stimuli (fully predictable vs. unpredictable deviants). We found deviance-related responses in both frequency bands over lateral temporal and inferior frontal cortex, with an earlier latency for Hγ than for LF-ERPs. Critically, frontal Hγ activity but not LF-ERPs discriminated between fully predictable and unpredictable changes, with frontal cortex sensitive to unpredictable events. The results highlight the role of frontal cortex and Hγ activity in deviance detection and PE generation.

AUTHORS

• S. Durschmid

• Erik Edwards

• Christoph Reichert

• Callum Dewar

• Hermann Hinrichs

• Hans-Jochen Heinze

• Heidi E. Kirsch

• Sarang S. Dalal

• Leon Y. Deouell

• Robert T. Knight

Date: 2016

DOI: 10.1073/pnas.1525030113

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